Comparative Craniometric Measurements of Two Sympatric Species of Vulpes in Ikh Nart Nature Reserve, Mongolia

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© 2018 Journal compilation ISSN 1684-3908 (print edition) http://mjbs.num.edu.mn Mongolian Journal of Biological http://biotaxa.org./mjbs Sciences MJBS Volume 16(1), 2018 ISSN 2225-4994 (online edition) http://dx.doi.org/10.22353/mjbs.2018.16.03 Original Article

Tserendorj Munkhzul1, Richard P. Reading2, Bayarbaatar Buuveibaatar3 & James D. Murdoch4

1Mammalian Ecology Laboratory, Institute of General and Experimental Biology, Mongolian Academy of Sciences, Ulaanbaatar, Mongolia 2International Conservation Coalition, Denver, Colorado 80220 USA, Butterfly Pavilion, Westminster, Colorado 80020 USA & Mongolian Conservation Coalition, Ulaanbaatar, Mongolia 3Wildlife Conservation Society, Mongolia Program, Ulaanbaatar, Mongolia 4Rubenstein School of Environment and Natural Resources, University of Vermont, George Aiken Center, Burlington, Vermont 05405 USA

Abstract

Key words: Corsac fox; In Mongolia, both the red fox (Vulpes vulpes) and corsac fox (Vulpes corsac) occupy cranium; morphometry; broad sympatric ranges, but despite their expansive ranges, few published details of red fox; Vulpes; skull. the craniometry of either species exist in Mongolia and other parts of northern and Article information: central Asia. To determine the morphological differences between two species of Received: 08 Febr. 2018 foxes, we tested for morphological and morphometrical differences between the red Accepted: 31 May 2018 (n = 13) and corsac (n = 11) foxes using 63 cranium measurements. All significantly Published online: different skull variables were larger for red foxes than corsac foxes. Thispaper 12 June 2018 reports comparison of the cranial measurements from skulls of red and corsac foxes Correspondence: and serves as a preliminary investigation of interspecific variation between these [email protected] species. Cite this paper as: Munkhzul, Ts., Reading, R. P., Buuveibaatar, B. & Murdoch, J. D. 2018. Comparative craniometric measurements of two sympatric species of Vulpes in Ikh Nart Nature Reserve, Mongolia. Mong. J. Biol. Sci., 16(1): 19-28.

Introduction

Red fox (Vulpes vulpes) and corsac fox requires knowledge of the species’ biology (Vulpes corsac) populations have declined and ecology, including especially the influence over recent years in Mongolia due to over- of poaching on population size and structure harvesting triggered by a high demand for furs (Murdoch et al., 2010b). and habitat degradation (Clark et al., 2006, The corsac fox differs in body size from Wingard & Zahler 2006). As a result, both sympatric congeners in the overlapping parts of species were designated under the IUCN Red their ranges. Corsac foxes may reach the body List Categories and Criteria as Near Threatened mass of the smallest red foxes, but generally regionally in 2006 (Clark et al., 2006), and corsac foxes are much smaller than red foxes, Least Concern globally more recently (Murdoch whose body mass ranges from 3-14 kg (Lariviere 2014; Hoffmann & Sillero-Zubiri 2016). Long- & Pasitschniak-Arts, 1996; Clark et al., 2009, term conservation of Mongolian fox populations Murdoch et al., 2009). Red foxes display sexual

19 20 Munkhzul et al. Craniometric measurements of two Vulpes species dimorphism in body weight and proportions from 140-150 mm (Lariviere & Pasitschniak- in many areas (Kolb & Hewson, 1974; Lups Arts, 1996, Clark et al., 2009). In addition, & Wandeler, 1983; Wandeler & Lups, 1993; corsac foxes have a less-developed and lower Macdonald & Sillero-Zubiri, 2004), including sagittal crest, a more gradually tapering rostrum, differences between male and female red fox and smaller, flatter auditory bullae than do red skulls from several different regions (Churcher, foxes (Sokolov & Orlov, 1980; Sheldon, 1992; 1960; Huson & Page, 1979; Lups & Wandeler, Clark et al., 2009). 1983; Fairly & Bruton, 1984; Hell et al., 1989; Ansorge, 1994; Lynch, 1996). Such dimorphism Materials and Methods could complicate comparisons between red and corsac foxes. Additional research found that We studied red and corsac fox samples parasites could modify skull dimensions in other obtained from skulls found opportunistically species (Demuth et al., 2009); however, whether and from radio-collared animals that died due or not this phenomenon occurs among foxes to poaching ornatural causes during ecological living in the wild, remain unknown. research in Ikh Nart Nature Reserve in Mongolia. Researchers have studied the morphology We collected 24 skull samples of red (n = 13) and craniometrics of red foxes and, to a lesser and corsac (n = 11) foxes in Ikh Nart between extent, corsac foxes in other parts of their ranges 2004 and 2008. The samples were stored (Ognev, 1962; Sokolov & Orlov, 1980; Churcher, in paper bags prior to transferring them to 1960; Huson & Page, 1979; Lups & Wandeler, the Mammalian Ecology Laboratory of the 1983; Fairly & Bruton, 1984; Hell et al., 1989; Institute of General and Experimental Biology, Ansorge, 1994; Lynch, 1996), but few published Mongolian Academy of Sciences. details exist on the cranial measurements of these We sorted the skulls by species; cleaned them species in Mongolia. Previous work found that of skin, flesh, and debris (mostly soil) and stored corsac foxes demonstrated a smaller total skull them in plastic bags. Skulls and mandibles were length than do red foxes, whose skulls range then soaked in antiseptic for 2 hours before

Figure 1. Measurements of the cranium of a fox Figure 2. Measurements of the cranium of a fox (Vulpes spp.) skull and dorsal view. See Table 1 for (Vulpes spp.) skull and basal view. See Table 1 for definitions of the abbreviations. definitions of the abbreviations.

Figure 3. Measurements of the cranium of a fox Figure 4. Measurements of the cranium of a fox (Vulpes spp.) skull and lateral view. See Table 1 for (Vulpes spp.) skull and nuchal view. See Table 1 for definitions of the abbreviations. definitions of the abbreviations. Mongolian Journal of Biological Sciences 2018 Vol. 16 (1-2) 21 collecting craniometric measurements. We measurements were provided in Table 1. used calipers for craniometry to an accuracy We also compared our results with other of 0.1 mm, following the skull measurement published data (Storm et al., 1976; Lynch, methods outlined by Von den Driesch (1976) 1996; Temizer, 2001). Following Grue and and Frackowiak et al. (2013). We gathered Jensen (1973), we counted cementum layers data on a total of 63 metric variables (Figures on longitudinally sanded canine roots as our 1-9). Definitions for the abbreviations of our primary procedure for age determination. Degree of fusion of cranial sutures, clothing of the tooth pulp, and the wear of the occlusal surface of M1 were used to confirm age determinations. Length parameters of the red fox skulls almost reach full size by 6 months of age, but width dimensions continue increasing until the second year of life

Figure 5. Measurements of the mandible of a fox Figure 6. Measurements of the maxillary and (Vulpes spp.) skull and lateral view. See Table 1 for mandibular teeth of a fox (Vulpes spp.) skull. See Table definitions of the abbreviations. 1 for definitions of the abbreviations.

Figure 7. Dorsal view of the skull of a) red fox (V. vulpes) and b) corsac fox (V. corsac) collected in Ikh Nart Nature Reserve, Mongolia. esc – external sagittal crest, ip – interparietal suture,tl– temporal line, if – interfrontalsuture, zp – zygomatic process, np – nasal processes.

Figure 8. Nuchal view of the skull of a) red fox (V. vulpes) and b) corsac fox (V. corsac) collected in Ikh Nart Nature Reserve, Mongolia. esc – external sagittal crest, nc – nuchal crest, spo– squamous part of the occipital bone, oc – occipital condyle, pp – paracondylar process, tb – tympanic bulla, fm – foramen magnum. 22 Munkhzul et al. Craniometric measurements of two Vulpes species

Table 1. Abbreviations of measurements made on red (V. vulpes) and corsac (V. corsac) fox skulls from Ikh Nart Nature Reserve, Mongolia. Actual measurements are illustrated in Figures 1-5.

Abbre- Measurement description Abbre- Measurement description viation viation Cranium measurements Ak-B: Height of the occipital triangle A-P: Total length B-Op: Height of the foramen magnum Ak-Fm: Upper neurocranium length BPp: Greatest breadth of the bases of the para- N-P: Viscerocranium length occipital processes Fm-P: Facial length BOc: Greatest breadth of the occipital condyles N-Rh: Greatest length of nasals BFm: Greatest breadth of the foramen magnum Or-P: “Snout” length Mandible measurements Zy-Zy: Zygomatic breadth Cp-I: Total length from condyle process NB: Greatest neurocranium breadth Ap-I: Length from angular process LBS: Least breadth of skull Cp-Ap: Length from indentation between the Ect-Ect: Frontal breadth condyle process and angularprocess Ent-Ent: Least breadth between the orbits Cp-Ca: Length from condyle process to the aboral border of the canine alveolus CbL: Condylobasal length LCp- Length from indentation between the B-P: Basal length Ap: condyle process and angularprocess to B-S: Basicranial axis the aboral border of the canine alveolus S-P: Basifacial axis Ap-Ca: Length from the angular process to the St-P: Median palatal length (see Figure 2) aboral border of the canine alveolus St-P*: Palatal length (see Figure 2) M3-Ca: Length from the aboral border of the alveolus of M to the aboral border ofthe St-Po: Length of the horizontal part of the pala- 3 tine (see Figure 2) canine alveolus St-Po*: Length of the horizontal part of the pala- M3-P1: Length of the cheektooth row tine (see Figure 2) M3-P2: Partial length of the cheektooth row LCR: Length of cheektooth row LMR: Length of the molar row LMr: Length of the molar row P1-P4: Length of the premolar row LPr: Length of the premolar row P2-P4: Partial length of the premolar row BCa: Breadth at the canine alveoli LBC: Length of the carnassials PB: Least palatal breadth LCA: Length of the carnassial alveolus

GPB: Greatest palatal breadth LM2: Length of M2

DAB: Greatest diameter of the auditory bulla LM3: Length of M3 BAm: Breadth dorsal to the external auditory HVR: Height of the vertical ramus meatus HM1: Height of the mandible behind M1 Sh: Skull height HP2-P3: Height of the mandible between P2 and P3 Sh*: Skull height without the sagittal crest Tooth measurements IHO: Greatest inner height of the orbit L: Maxillary and mandibular tooth length Ot-Ot: Greatest mastoid breadth B: Maxillary and mandibular tooth breadth

(Ansorge, 1994). We defined age classes as: 1 and 5 years for both species. We pooled all 1 to < 2 years, 2 to < 3 years, 3 to < 4 years, measurements across all age classes for both 4 to < 5 years, and 5 years and older. We were species for comparison. able to determine ages for 9 red fox skulls and We collected basic descriptive statistics, 6 corsac fox skulls. An average (± SD) age of including the mean, standard deviation (SD), red and corsac fox skulls were 4.15 ± 1.36 and and coefficient of variation (CV). We used the 3.17 ± 1.83 years, respectively, ranged between non-parametric Wilcoxon-Matt-Whitney U-test, Mongolian Journal of Biological Sciences 2018 Vol. 16 (1-2) 23

Figure 9. Lateral view of the mandible of a) red fox (V. vulpes) and b) corsac fox (V. corsac) collected in Ikh Nart Nature Reserve, Mongolia. vm – ventral margin of the body of the mandible – bm, mf – mental foramen, mfo – masseteric fossa, mn – mandibular notch, ap – angular process. similar to a t-test for independent samples, to developed than in the corsac fox (Figures 7 and compare cranial measurements between species 8). The upper side of the foramen magnum was because our data did not follow a normal wider and more arched of the red fox, while that distribution. We analyzed data using R (R Core of the corsac foxes was more oval (Figure 8). Team 2015) and significance was set at P < 0.05. Both species have two mental foramina of the mandible (Figure 9). Red foxes’ masseteric Results fossa was deeper and wider than in corsac foxes. In addition, the mandibular notch and angular We found significantly different skull process were slightly better developed in the measurements for most morphological features red fox (Figure 9). Red foxes “lower edge of the between corsac foxes and red foxes. In ramus curved gently back to the end of the angle, particular, corsac foxes demonstrated smaller, but corsac foxes” lower edge of ramus showed a shorter and wider skulls, and with more robust distinct step, or break, just in front of the angle canine teeth (Table 2). The corsac fox possessed (Figure 9). a more gradually tapering rostrum and smaller, Skull morphological measurements confirmed flatter auditory bullae than did the red fox these visual differences. We found significant (Figure 7). The external sagittal crest of the red differences in most skull measurements between fox arises at the junction of the temporal lines, two species (Table 2). In particular, measurements near the interparietal bone (Figure 7a). The from the basal view (LPr, DAB, GPB), dorsal interfrontal and interparietal sutures in the red fox view (NB), nichal view (Ot-ot), laterial view running between temporal lines were typically (Hp-I, Cp-Ap, Cp-Ca, LCa-Ap, Ap-Ca, M3-Ca, serrated. Low ridges extended back from the LMR, LCA) and maxillary teeth (M1L) showed postorbital processes, with the temporal lines of highly significant differences (Table 2). Similarly, the postorbital processes converging at an acute most of the dental measurements of the skull and angle at the boundary of the frontal and parietal mandible revealed highly significant differences bones and forming a “V” shape on top of the between species (Table 2). Most measurements skull (Figure 7a). Alternatively, in corsac foxes of the length of the mandible (HP-I, Cp-Ap, the temporal lines diverged from the postorbital Cp-Ca, LCa-Ap, Ap-Ca, M3-Ca) revealed processes, ran nearly parallel on top of the skull significant differences between species (Table 2). (with an under-developed interparietal suture), Measurements of the posterior part of the body and converged near the posterior suture of the of mandible (LCA, HM1) revealed significant parietal bones (Figure 7b). Further, the corsac fox differences between species (Table 2). had a less-developed and lower external sagittal and nuchal crests than did the red fox (Figures 7 Discussion & 8). The squamous part of the occipital bone in the Coexistence of species that occupy similar corsac fox was smaller than in the red fox (Figure niches generally occurs through the differential 7). The occipital condyles, paracondylar process use of resources, such as food, space, and time and tympanic bullae in the red fox were all better (Schoener, 1974). Such resource partitioning 24 Munkhzul et al. Craniometric measurements of two Vulpes species

Table 2. Comparison of mean (± SD) measurements (cm) of red (V. vulpes) and corsac (V. corsac) fox skulls, mandibles, and teeth from Ikh Nart Nature Reserve, Mongolia. Differences examinedWilcox Mann Whitney U test.

Red fox Corsac fox View Measurement W P N Mean ± SD CV N Mean ± SD CV Dorsal view A-P 12 14.7 ± 0.6 0.04 11 12.08 ± 1.3 0.1 126 <0.001 Fm-P 13 8.2 ± 0.4 0.05 11 6.6 ± 0.8 0.1 134 <0.001 Ak-Fm 12 6.8 ± 0.4 0.06 11 5.8 ± 0.3 0.05 122 <0.001 N-P 13 6.9 ± 0.4 0.06 11 5.5 ± 0.7 0.13 132 <0.001 N-Rh 13 5.4 ± 0.3 0.06 11 4.3 ± 0.6 0.1 120 <0.001 Or-P 13 6.04 ± 0.4 0.07 11 4.6 ± 0.6 0.1 133 <0.001 NB 12 4.7 ± 0.2 0.04 11 4.3 ± 0.1 0.03 122 <0.001 Zy-Zy 8 7.6 ± 0.3 0.04 9 6.7 ± 0.5 0.08 65 <0.005 LBS 12 2.2 ± 0.1 0.05 11 2.3 ± 0.1 0.08 50 <0.5 Ect 13 3.5 ± 0.3 0.1 11 3.1 ± 0.3 0.1 109 <0.05 Ent 13 2.7 ± 0.2 0.07 11 2.4 ± 0.2 0.1 109 <0.05 Basal view CBL 12 14.04 ± 0.7 0.05 10 11.7 ± 1.3 0.1 107 <0.001 B-P 12 12.7 ± 1.4 0.11 11 11.0 ± 1.3 0.1 105 <0.01 B-S 10 3.6 ± 0.3 0.08 11 2.6 ± 0.4 0.1 102 <0.001 S-P 10 9.7 ± 0.9 0.09 11 8.2 ± 0.9 0.1 92 <0.01 St-P 12 7.2 ± 0.4 0.05 11 6.05 ± 0.7 0.1 120 <0.001 St*-P 12 7.05 ± 0.3 0.05 11 5.8 ± 0.6 0.1 120 <0.001 St-Po 12 2.1 ± 0.4 0.2 11 1.9 ± 0.3 0.2 108 <0.01 St*Po 12 2.04 ± 0.1 0.08 11 1.8 ± 0.2 0.2 108 <0.01 LCR 12 5.4 ± 0.2 0.04 11 4.5 ± 0.5 0.1 118 <0.001 LMr 13 1.3 ± 0.1 0.1 11 1.1 ± 0.2 0.2 116 <0.01 LPr 12 4.2 ± 0.1 0.04 11 3.6 ± 0.4 0.1 116 <0.005 DAB 11 2.1 ± 0.06 0.02 11 1.8 ± 0.1 0.1 60 <0.001 Ot 12 4.7 ± 0.2 0.04 11 4.1 ± 0.4 0.09 117 <0.001 GPB 13 4.0 ± 0.2 0.06 11 3.5 ± 0.3 0.08 124 <0.005 Lateral view Cp-I 8 9.6 ± 3.3 0.3 7 9.1 ± 0.8 0.09 47 <0.05 HP-I 12 10.8 ± 0.5 0.04 11 8.9 ± 0.7 0.08 128 <0.001 Cp-Ap 12 10.4 ± 0.5 0.04 11 8.8 ± 0.9 0.1 118 <0.001 Cp-Ca 13 9.9 ± 0.3 0.03 10 8.2 ± 0.7 0.08 114 <0.001 LCa-Ap 11 9.3 ± 0.3 0.03 9 7.8 ± 0.6 0.08 97 <0.001 Ap-Ca 13 9.6 ± 0.4 0.05 11 8.07 ± 0.6 0.07 138 <0.001 M3-Ca 13 6.5 ± 0.2 0.03 11 5.4 ± 0.4 0.08 136 <0.001 M3-P1 12 5.9 ± 0.2 0.04 11 5.0 ± 0.4 0.08 123 <0.001 M3-P2 13 5.4 ± 0.2 0.03 11 4.5 ± 0.4 0.09 136 <0.001 LMR 13 2.6 ± 0.1 0.03 11 2.1 ± 0.1 0.09 141 <0.001 P1-P4 13 3.5 ± 0.2 0.08 9 2.9 ± 0.2 0.07 106 <0.01 P2-P4 12 2.7 ± 0.3 0.1 11 2.4 ± 0.2 0.08 116 <0.001 LBC 13 1.6 ± 0.2 0.1 10 1.3 ± 0.1 0.1 116 <0.001 LCA 13 1.3 ± 0.09 0.06 10 1.08 ± 0.1 0.1 122 <0.001 HVR 13 3.7 ± 0.1 0.04 11 3.2 ± 0.2 0.06 137 <0.001 HM1 13 1.4 ± 0.07 0.04 10 1.2 ± 0.1 0.1 125 <0.001 HP2-P3 11 1.4 ± 0.2 0.1 10 1.05 ± 0.09 0.08 97 <0.005 Left side IHO 11 2.2 ± 0.4 0.1 10 2.2 ± 0.07 0.03 63 <0.5 view Sh 12 4.0 ± 0.3 0.08 11 3.7 ± 0.6 0.1 93 <0.1 Sh* 12 3.7 ± 0.3 0.09 11 3.5 ± 0.5 0.1 83 <0.5 Mongolian Journal of Biological Sciences 2018 Vol. 16 (1-2) 25

Table 2. (continued)

Red fox Corsac fox View Measurement W P N Mean ± SD CV N Mean ± SD CV Nichal view Ot-Ot 11 4.8 ± 0.1 0.02 11 4.2 ± 0.3 0.08 114 <0.001 BFm 12 1.5 ± 0.03 7.3 11 1.3 ± 0.3 8.2 115 <0.005 BOc 12 2.5 ± 0.07 0.02 11 2.2 ± 0.3 0.1 107 <0.01 BPp 11 4.1 ± 0.4 0.1 10 3.6 ± 0.3 0.09 91 <0.01 B-Op 12 1.1 ± 0.05 0.05 10 0.9 ± 0.07 0.07 108 <0.001 AK-B 12 2.5 ± 0.1 0.06 11 2.2 ± 0.2 0.09 108 <0.005 Tooth view Max-P4L 9 1.4 ± 0.1 0.1 10 1.2 ± 0.1 0.1 84 <0.05 Max -P4B 10 0.6 ± 0.1 0.2 10 0.5 ± 0.05 0.1 92 <0.01 Max -M1L 11 0.9 ± 0.09 0.1 10 0.7 ± 0.2 0.2 113 <0.005 Max -M1B 10 1.2 ± 0.08 0.06 10 1.04 ± 0.1 0.1 108 <0.01 Max -M2L 10 0.5 ± 0.04 0.08 10 0.4 ± 0.04 0.09 86 <0.001 Max-M2B 10 0.7 ± 0.2 0.2 10 0.7 ± 0.09 0.1 74 <0.05 Man-M1L 8 1.5 ± 0.2 0.1 8 1.2 ± 0.1 0.1 54 <0.01 Man-M1B 8 0.6 ± 0.08 0.1 8 0.4 ± 0.07 0.1 45 <0.5 Man -M2L 8 0.7 ± 0.02 0.03 8 0.5 ± 0.09 0.1 52 <0.05 Man -M2B 8 0.4 ± 0.2 0.3 8 0.4 ± 0.07 0.01 51 <0.05 Man-M3L 6 0.3 ± 0.04 0.1 8 0.2 ± 0.03 0.1 43 <0.01 Man-M3B 8 0.3 ± 0.03 0.1 8 0.2 ± 0.05 0.2 38 <0.05 reduces competition and may be inferred from mammalian guide books provide different morphological differentiation (Begon et al., guidelines for distinguishing between red and 2006). Red and corsac foxes occur sympatrically corsac foxes using skull morphology. Bannikov in Ikh Nart Nature Reserve and other arid steppe (1954), Dulamtseren (1970) and Batsaikhan et regions of Mongolia (Clark et al., 2006), and al. (2010) suggested that skulls greater than 130 occupy similar ecological niches (Murdoch et al., mm in length come from red foxes, while skulls 2007; Murdoch, 2009; Munkhzul et al., 2012). less than 130 mm in length come from corsac Mammalian skulls are highly informative, foxes. Heptner et al. (1992) stated that corsac fox conservative, and adaptive structures, and skull lengths range between 95 and 112 mm and therefore, represent a powerful tool for suggested if the total length of skull is >115 mm biogeographic, phylogenetic, and systematic then it comes from a red fox. In addition, Sokolov investigations, especially in the absence of & Orlov (1980) reported that the total length of molecular investigations (Loy, 2007). The Vulpes red fox skulls varied between 130 and 160 mm. skulls available in museum and private collections In a comparative study of the skulls of red fox could reveal a mass of information related to and arctic foxes (Vulpes lagopus), Frackowiak et the adaptations of these animals. A large part al. (2013) found the most distinct morphological of the systematic structure of red foxes in the differences in the nasal, temporal, parietal steppe area has been constructed on the grounds and occipital bones. They found that the most of these skulls, especially at the subspecies important morphological differences occurred level. Researchers have identified some skull within craniometric measurements, especially in morphological differences between red and the nasal, occipital, and temporal bones, and the corsac foxes (Bannikov, 1954; Sokolov & Orlov, parietal, maxilla, and mandible areas. 1980), but relatively few publications compare Influences of individual age on the red and corsac fox skull morphologies. Similarly, craniometric measurements of both species were we are unaware of any studies that compare the noticeable in our study. Specifically, we observed craniums of both species. Russian and Mongolian a more developed external sagittal crest, wider 26 Munkhzul et al. Craniometric measurements of two Vulpes species

Table 3. Mean (± SE) craniometric measurements (cm) of corsac foxes (V. corsac) from northern Kazakhstan (Kadyrbaev and Sludskii 1981), Turkmenstan (Scherbina 1995) and Mongolia.

Measurement Kazakhstan (n=22) Turkmenstan (n=9) Ikh Nart (n=11) Skull length 10.6 10.7 12.07 ± 0.3 Zygomatic breadth 6.1 6.4 6.7 ± 0.2 Height of auditory bullae 4.2 4.4 4.6 ± 0.3 Upper row of teeth 4.0 5.2 4.6 ± 0.4 more arched foramen magnum, deeper and south to China along with virtually all other wider masseteric fossa, and better developed forms of wildlife trade (Wingard & Zahler, 2006). mandibular notch and angular process in red foxes Overhunting, coupled with habitat disturbance, than in corsac foxes. Jurgelenas et al. (2007) and has caused the corsac fox to disappear from much Frackowiak et al. (2013) found similar patterns of its historic range (Ognev, 1962; Stroganov, in their comparison of the skulls of the red fox, 1962). The current level of trade in Mongolia has raccoon dog (Nyctereutes procyonoides; Hidaka the potential to similarly impact the both species et al. 1998) and arctic fox. Our study showed and results from our study can be used to help differences in the almost all measurements of identify poached foxes to species level. both species particularly length of the molar row of maxilla and mandible. We also found age and Acknowledgments species differences in the skulls of both species in Mongolia. This study was supported and funded by Craniometric comparisons of corsac foxes the Denver Zoological Foundation, Mongolian from Ikh Nart with animals from Kazakhstan Conservation Coalition, Rufford Foundation, and Turkmenistan suggest agreement with Trust for Mutual Understanding, Earthwatch Bergmann’s rule (Table 3). However, sample Institute and Mongolian Academy of Sciences, sizes from all three populations were relatively Institute of General and Experimental Biology. small and more samples, particularly from other We thank B. Otgonbayar and D. Choibalsan for regions, would be helpful for assessing whether their help in obtaining red and corsac fox skulls. latitudinal clines exist. Male corsac foxes in Ikh For edits and comments, we are grateful to E. Nart, for example, were lighter on average than Cheng, B. Lhagvasuren and H. Ansorge. males at a more northern latitude in Kazakhstan, but heavier than those from a site to the south References in Turkmenistan (Kadyrbaev & Sludskii, 1981; Scherbina, 1995; Murdoch et al., 2009). Corsac Ansorge, H. 1994. Intrapopular skull variability foxes from Turkmenistan had longer mean in the red fox, Vulpes vulpes (Mammalia body lengths with shorter mean tail lengths Carnivore: Canidae). Zoology of Abh. Staat. than those from northern Kazakhstan and Ikh Mus. Tierk. Dresden, 48: 103-123. Nart, contradicting Allen’s Rule (Kadyrbaev & Bannikov, A.G. 1954. Identification Key to Sludskii, 1981; Scherbina, 1995; Murdoch et al., the Mammals of the Mongolian People’s 2009). Republic. Mockow. pp. 122-134. (In Russian) Corsac fox and red fox has been a staple Batsaikhan, N., Samiya, R., Shar, S., source of fur in Mongolia for many years Lkhagvasuren, D. & King, S.R.B. 2014. A (Wingard & Zahler, 2006). In 1973, concerns that Field Guide to the Mammals of Mongolia. harvest levels had been unsustainable for many Ulaanbaatar. Pp 222-224. (In Mongolian and years caused the Mongolian government to ban English) trade in corsac fox furs. It was never reinstated Begon, M., Townsend, C.R., Harper, J.L. 2006. under the communist system. In the 1990, Ecology from individuals to ecosystems. - 4th Mongolians once again started harvesting this edition, Blackwell Publishing, Oxford, UK. small carnivore to sell on the international market. Churcher, C.S. 1960. Cranial variation in With the shift in government, trade went primarily the North American red fox. Journal of Mongolian Journal of Biological Sciences 2018 Vol. 16 (1-2) 27

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